Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-17T02:47:33.124Z Has data issue: false hasContentIssue false

Prefrontal and Hippocampal Brain Volume Deficits: Role of Low Physical Activity on Brain Plasticity in First-Episode Schizophrenia Patients

Published online by Cambridge University Press:  19 November 2015

Sarah C. McEwen*
Affiliation:
Department of Psychiatry & Biobehavioral Sciences, University of California, Los Angeles, California
Anthony Hardy
Affiliation:
Department of Radiology, University of California, Los Angeles, California
Benjamin M. Ellingson
Affiliation:
Department of Psychiatry & Biobehavioral Sciences, University of California, Los Angeles, California Department of Radiology, University of California, Los Angeles, California
Behnaz Jarrahi
Affiliation:
Department of Psychiatry & Biobehavioral Sciences, University of California, Los Angeles, California
Navjot Sandhu
Affiliation:
Department of Psychiatry & Biobehavioral Sciences, University of California, Los Angeles, California
Kenneth L. Subotnik
Affiliation:
Department of Psychiatry & Biobehavioral Sciences, University of California, Los Angeles, California
Joseph Ventura
Affiliation:
Department of Psychiatry & Biobehavioral Sciences, University of California, Los Angeles, California
Keith H. Nuechterlein
Affiliation:
Department of Psychiatry & Biobehavioral Sciences, University of California, Los Angeles, California Department of Psychology, University of California, Los Angeles, California
*
Correspondence and reprint requests to: Sarah McEwen, University of California, Los Angeles, 760 Westwood Plaza, Mail Code: 696825, Los Angeles, CA 90095. E-mail: [email protected]

Abstract

Our objective in the present study was to conduct the first empirical study of the effects of regular physical activity habits and their relationship with brain volume and cortical thickness in patients in the early phase of schizophrenia. Relationships between larger brain volumes and higher physical activity levels have been reported in samples of healthy and aging populations, but have never been explored in first-episode schizophrenia patients. Method: We collected MRI structural scans in 14 first-episode schizophrenia patients with either self-reported low or high physical activity levels. We found a reduction in total gray matter volume, prefrontal cortex (PFC), and hippocampal gray matter volumes in the low physical activity group compared to the high activity group. Cortical thickness in the dorsolateral and orbitofrontal PFC were also significantly reduced in the low physical activity group compared to the high activity group. In the combined sample, greater overall physical activity levels showed a non-significant tendency with better performance on tests of verbal memory and social cognition. Together these pilot study findings suggest that greater amounts of physical activity may have a positive influence on brain health and cognition in first-episode schizophrenia patients and support the implementation of physical exercise interventions in this patient population to improve brain plasticity and cognitive functioning. (JINS, 2015, 21, 868–879)

Type
Research Article
Copyright
Copyright © The International Neuropsychological Society 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdel-Baki, A., Brazzini-Poisson, V., Marois, F., Letendre, E., & Karelis, A.D. (2013). Effects of aerobic interval training on metabolic complications and cardiorespiratory fitness in young adults with psychotic disorders: A pilot study. Schizophrenia Research, 149(1-3), 112115.CrossRefGoogle ScholarPubMed
Adams, L. (1994). How exercise can help people with mental health problems. Nursing Times, 91(36), 3739.Google Scholar
American Psychiatric Association (1994). Diagnostic and Statistical Manual of Mental Disorders (DSM-IV). Washington, DC: American Psychiatric Press.Google Scholar
Åstrand, P., & Saltin, B. (1961). Oxygen uptake during the first minutes of heavy muscular exercise. Journal of Applied Physiology, 16(6), 971976.Google ScholarPubMed
Bassett, D.R., & Howley, E.T. (2000). Limiting factors for maximum oxygen uptake and determinants of endurance performance. Medicine and Science in Sports and Exercise, 32(1), 7084.CrossRefGoogle ScholarPubMed
Beebe, L.H., Tian, L., Morris, N., Goodwin, A., Allen, S.S., & Kuldau, J. (2005). Effects of exercise on mental and physical health parameters of persons with schizophrenia. Issues in Mental Health Nursing, 26(6), 661676.CrossRefGoogle ScholarPubMed
Brown, S., Kim, M., Mitchell, C., & Inskip, H. (2010). Twenty-five year mortality of a community cohort with schizophrenia. The British Journal of Psychiatry, 196(2), 116121.CrossRefGoogle ScholarPubMed
Colcombe, S., & Kramer, A.F. (2003). Fitness effects on the cognitive function of older adults a meta-analytic study. Psychological Science, 14(2), 125130.CrossRefGoogle ScholarPubMed
Colcombe, S.J., Erickson, K.I., Scalf, P.E., Kim, J.S., Prakash, R., McAuley, E., & Kramer, A.F. (2006). Aerobic exercise training increases brain volume in aging humans. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 61(11), 11661170.CrossRefGoogle ScholarPubMed
Cotman, C.W., Berchtold, N.C., & Christie, L.A. (2007). Exercise builds brain health: Key roles of growth factor cascades and inflammation. Trends in Neurosciences, 30(9), 464472.CrossRefGoogle Scholar
Craig, C.L., Marshall, A.L., Sjöström, M., Bauman, A.E., Booth, M.L., Ainsworth, B.E., & Oja, P. (2003). International physical activity questionnaire: 12-country reliability and validity. Medicine and Science in Sports and Exercise, 35(8), 13811395.CrossRefGoogle ScholarPubMed
Dale, A.M., Fischl, B., & Sereno, M.I. (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage, 9(2), 179194.CrossRefGoogle ScholarPubMed
Dale, A.M., & Sereno, M.I. (1993). Improved localizadon of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: A linear approach. Journal of Cognitive Neuroscience, 5(2), 162176.CrossRefGoogle ScholarPubMed
Day, J.R., Rossiter, H.B., Coats, E.M., Skasick, A., & Whipp, B.J. (2003). The maximally attainable VO2 during exercise in humans: The peak vs. maximum issue. Journal of Applied Physiology, 95(5), 19011907.CrossRefGoogle ScholarPubMed
De Hert, M., Dekker, J., Wood, D., Kahl, K., Holt, R., & Möller, H.J. (2009). Cardiovascular disease and diabetes in people with severe mental illness position statement from the European Psychiatric Association (EPA), supported by the European Association for the Study of Diabetes (EASD) and the European Society of Cardiology (ESC). European Psychiatry, 24(6), 412424.CrossRefGoogle Scholar
De Hert, M., Detraux, J., Van Winkel, R., Yu, W., & Correll, C.U. (2012). Metabolic and cardiovascular adverse effects associated with antipsychotic drugs. Nature Reviews Endocrinology, 8(2), 114126.CrossRefGoogle Scholar
De Hert, M., Schreurs, V., Vancampfort, D., & Winkel, R. (2009). Metabolic syndrome in people with schizophrenia: A review. World Psychiatry, 8(1), 1522.CrossRefGoogle ScholarPubMed
Erickson, K.I., Miller, D.L., & Roecklein, K.A. (2012). The aging hippocampus: Interactions between exercise, depression, and BDNF. Neuroscientist, 18(1), 8297.CrossRefGoogle ScholarPubMed
Falkai, P., Malchow, B., Wobrock, T., Gruber, O., Schmitt, A., Honer, W.G., & Cannon, T.D. (2013). The effect of aerobic exercise on cortical architecture in patients with chronic schizophrenia: A randomized controlled MRI study. European Archives of Psychiatry and Clinical Neuroscience, 263(6), 469473.CrossRefGoogle ScholarPubMed
Faulkner, G., & Carless, D. (2006). Physical activity in the process of psychiatric rehabilitation: Theoretical and methodological issues. Psychiatric Rehabilitation Journal, 29(4), 258.CrossRefGoogle ScholarPubMed
Faulkner, G., Cohn, T., & Remington, G. (2006). Validation of a physical activity assessment tool for individuals with schizophrenia. Schizophrenia Research, 82(2-3), 225231.CrossRefGoogle ScholarPubMed
Firth, J., Cotter, J., Elliott, R., French, P., & Yung, A.R. (2015). A systematic review and meta-analysis of exercise interventions in schizophrenia patients. Psychological Medicine, 45(7), 13431361.CrossRefGoogle ScholarPubMed
Fischl, B., & Dale, A.M. (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences of the United States of America, 97(20), 1105011055.CrossRefGoogle ScholarPubMed
Fischl, B., Salat, D.H., Busa, E., Albert, M., Dieterich, M., Haselgrove, C., & Dale, A.M. (2002). Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron, 33(3), 341355.CrossRefGoogle ScholarPubMed
Fischl, B., Sereno, M.I., & Dale, A.M. (1999). Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage, 9(2), 195207.CrossRefGoogle Scholar
Fischl, B., Sereno, M.I., Tootell, R.B., & Dale, A.M. (1999). High-resolution intersubject averaging and a coordinate system for the cortical surface. Human Brain Mapping, 8(4), 272284.3.0.CO;2-4>CrossRefGoogle Scholar
Fritz-Wieacker, A., Matschinger, H., Heider, D., Schindler, J., Riedel-Heller, S., & Angermeyer, M.C. (2007). Health habits of patients with schizophrenia. Social Psychiatry and Psychiatric Epidemiology, 42(4), 268276.Google Scholar
Gomez‐Pinilla, F., Vaynman, S., & Ying, Z. (2008). Brain‐derived neurotrophic factor functions as a metabotrophin to mediate the effects of exercise on cognition. European Journal of Neuroscience, 28(11), 22782287.CrossRefGoogle ScholarPubMed
Gorczynski, P., & Faulkner, G. (2010). Exercise therapy for schizophrenia. Cochrane Database Syst Rev, 5, CD004412. doi:10.1002/14651858.CD004412.pub2.Google ScholarPubMed
Hausswolff-Juhlin, V., Bjartveit, M., Lindström, E., & Jones, P. (2009). Schizophrenia and physical health problems. Acta Psychiatrica Scandinavica, 119(s438), 1521.CrossRefGoogle Scholar
Heggelund, J., Hoff, J., Helgerud, J., Nilsberg, G.E., & Morken, G. (2011). Reduced peak oxygen uptake and implications for cardiovascular health and quality of life in patients with schizophrenia. BMC Psychiatry, 11(188), 18.CrossRefGoogle ScholarPubMed
Heggelund, J., Kleppe, K.D., Morken, G., & Vedul-Kjelsås, E. (2014). High aerobic intensity training and psychological states in patients with depression or schizophrenia. Frontiers in Psychiatry, 5(148), 18.CrossRefGoogle ScholarPubMed
Heggelund, J., Nilsberg, G.E., Hoff, J., Morken, G., & Helgerud, J. (2011). Effects of high aerobic intensity training in patients with schizophrenia-A controlled trial. Nordic Journal of Psychiatry, 65(4), 269275.CrossRefGoogle ScholarPubMed
Hennekens, C.H. (2006). Increasing global burden of cardiovascular disease in general populations and patients with schizophrenia. The Journal of Clinical Psychiatry, 68, 47.Google Scholar
Hillman, C.H., Erickson, K.I., & Kramer, A.F. (2008). Be smart, exercise your heart: Exercise effects on brain and cognition. Nature Reviews Neuroscience, 9(1), 5865.CrossRefGoogle ScholarPubMed
Joukamaa, M.M., Heliövaara, M., Knekt, P., Aromaa, A., Raitasalo, R., & Lehtinen, V. (2006). Schizophrenia, neuroleptic medication and mortality. The British Journal of Psychiatry, 188(2), 122127.CrossRefGoogle ScholarPubMed
Kim, H.J., Song, B.K., So, B., Lee, O., Song, W., & Kim, Y. (2014). Increase of circulating BDNF levels and its relation to improvement of physical fitness following 12 weeks of combined exercise in chronic patients with schizophrenia: A pilot study. Psychiatry Research, 220(3), 792796.CrossRefGoogle ScholarPubMed
Kimhy, D., Vakhrusheva, J., Bartels, M.N., Armstrong, H.F., Ballon, J.S., Khan, S., & Sloan, R.P. (2015). The impact of aerobic exercise on brain-derived neurotrophic factor and neurocognition in individuals with schizophrenia: A single-blind, randomized clinical trial. Schizophrenia Bulletin, 41, 859868. doi:10.1093/schbul/sbv022.CrossRefGoogle ScholarPubMed
Krogh, J., Speyer, H., Nørgaard, H.C.B., Moltke, A., & Nordentoft, M. (2014). Can exercise increase fitness and reduce weight in patients with schizophrenia and depression? Frontiers in Psychiatry, 5(89), 16.CrossRefGoogle ScholarPubMed
Lee, E.H., Hui, C.L., Chang, W.C., Chan, S.K., Li, Y., Lee, J.T., & Chen, E.Y. (2013). Impact of physical activity on functioning of patients with first-episode psychosis—A 6 months prospective longitudinal study. Schizophrenia Research, 150(2), 538541.CrossRefGoogle ScholarPubMed
Lindamer, L.A., McKibbin, C., Norman, G.J., Jordan, L., Harrison, K., Abeyesinhe, S. & Patrick, K. (2008). Assessment of physical activity in middle-aged and older adults with schizophrenia. Schizophrenia Research, 104(1), 294301.CrossRefGoogle ScholarPubMed
Malchow, B., Keller, K., Hasan, A., Dörfler, S., Schneider-Axmann, T., Hillmer-Vogel, U., & Falkai, P. (2015). Effects of endurance training combined with cognitive remediation on everyday functioning, symptoms, and cognition in multiepisode schizophrenia patients. Schizophrenia Bulletin, doi:10.1093/schbul/sbv020 CrossRefGoogle ScholarPubMed
Malchow, B., Reich-Erkelenz, D., Oertel-Knöchel, V., Keller, K., Hasan, A., Schmitt, A., & Falkai, P. (2013). The effects of physical exercise in schizophrenia and affective disorders. European Archives of Psychiatry and Clinical Neuroscience, 263(6), 451467.CrossRefGoogle ScholarPubMed
Maud, P.J., & Foster, C. (2006). Physiological Assessment of Human Fitness (2nd edition). Champaign, IL: Human Kinetics.Google Scholar
McCreadie, R.G. (2003). Diet, smoking and cardiovascular risk in people with schizophrenia Descriptive study. The British Journal of Psychiatry, 183(6), 534539.Google ScholarPubMed
McGrath, J., Saha, S., Chant, D., & Welham, J. (2008). Schizophrenia: A concise overview of incidence, prevalence, and mortality. Epidemiologic Reviews, 30(1), 6776.CrossRefGoogle ScholarPubMed
Mitchell, A.J., Vancampfort, D., Sweers, K., Van Winkel, R., Yu, W., & De Hert, M. (2013). Prevalence of metabolic syndrome and metabolic abnormalities in schizophrenia and related disorders—a systematic review and meta-analysis. Schizophrenia Bulletin, 39(2), 306318.CrossRefGoogle ScholarPubMed
Mitchell, J.H., Sproule, B.J., & Chapman, C.B. (1958). The physiological meaning of the maximal oxygen intake test. Journal of Clinical Investigation, 37(4), 538.CrossRefGoogle ScholarPubMed
Mittal, V.A., Gupta, T., Orr, J.M., Pelletier-Baldelli, A., Dean, D.J., Lunsford-Avery, J., & Millman, Z.B. (2013). Physical activity level and medial temporal health in youth at ultra high-risk for psychosis. Journal of Abnormal Psychology, 122(4), 11011110.CrossRefGoogle ScholarPubMed
Neeper, S., Gómez-Pinilla, A.F., Choi, J., & Cotman, C. (1995). Exercise and brain neurotrophins. Nature, 373(6510), 109.CrossRefGoogle ScholarPubMed
Newcomer, J.W. (2005). Second-generation (atypical) antipsychotics and metabolic effects. CNS Drugs, 19(1), 193.CrossRefGoogle ScholarPubMed
Newman, S.C., & Bland, R.C. (1991). Mortality in a cohort of patients with schizophrenia: A record linkage study. The Canadian Journal of Psychiatry/La Revue Canadienne de Psychiatrie, 36(4), 239245.CrossRefGoogle Scholar
Nuechterlein, K.H., Barch, D.M., Gold, J.M., Goldberg, T.E., Green, M.F., & Heaton, R.K. (2004). Identification of separable cognitive factors in schizophrenia. Schizophrenia Research, 72(1), 2939.CrossRefGoogle ScholarPubMed
Nuechterlein, K.H., Green, M.F., Kern, R.S., Baade, L.E., Barch, D.M., Cohen, J.D., & Marder, S.R. (2008). The MATRICS Consensus Cognitive Battery, part 1: Test selection, reliability, and validity. American Journal of Psychiatry, 165(2), 203213.CrossRefGoogle ScholarPubMed
Pajonk, F.G., Wobrock, T., Gruber, O., Scherk, H., Berner, D., Kaizl, I., & Meyer, T. (2010). Hippocampal plasticity in response to exercise in schizophrenia. Archives of General Psychiatry, 67(2), 133143.CrossRefGoogle ScholarPubMed
Paxton, A.E., Strycker, L.A., Toobert, D.J., Ammerman, A.S., & Glasgow, R.E. (2011). Starting the conversation performance of a brief dietary assessment and intervention tool for health professionals. American Journal of Preventive Medicine, 40(1), 6771.CrossRefGoogle ScholarPubMed
Pelham, T.W., Campagna, P.D., Ritvo, P.G., & Birnie, W.A. (1993). The effects of exercise therapy on clients in a psychiatric rehabilitation program. Psychosocial Rehabilitation Journal, 16(4), 7584.CrossRefGoogle Scholar
Pereira, A.C., Huddleston, D.E., Brickman, A.M., Sosunov, A.A., Hen, R., McKhann, G.M., & Small, S.A. (2007). An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proceedings of the National Academy of Sciences of the United States of America, 104(13), 56385643.CrossRefGoogle Scholar
Poo, M.M. (2001). Neurotrophins as synaptic modulators. Nature Reviews Neuroscience, 2(1), 2432.CrossRefGoogle ScholarPubMed
Prince, S.A., Adamo, K.B., Hamel, M.E., Hardt, J., Gorber, S.C., & Tremblay, M. (2008). A comparison of direct versus self-report measures for assessing physical activity in adults: A systematic review. The International Journal of Behaviioral Nutrition and Physical Activity, 5, 56.CrossRefGoogle ScholarPubMed
Rosenbaum, S., Tiedemann, A., Sherrington, C., Curtis, J., & Ward, P.B. (2014). Physical activity interventions for people with mental illness: A systematic review and meta-analysis. The Journal of Clinical Psychiatry, 75(9), 964974.CrossRefGoogle ScholarPubMed
Saha, S., Chant, D., & McGrath, J. (2007). A systematic review of mortality in schizophrenia: Is the differential mortality gap worsening over time? Archives of General Psychiatry, 64(10), 11231131.CrossRefGoogle ScholarPubMed
Salat, D.H., Buckner, R.L., Snyder, A.Z., Greve, D.N., Desikan, R.S., Busa, E., & Fischl, B. (2004). Thinning of the cerebral cortex in aging. Cerebral Cortex, 14(7), 721730.CrossRefGoogle ScholarPubMed
Scheewe, T., Backx, F., Takken, T., Jörg, F., Strater, A. V., Kroes, A., & Cahn, W. (2013). Exercise therapy improves mental and physical health in schizophrenia: A randomised controlled trial. Acta Psychiatrica Scandinavica, 127(6), 464473.CrossRefGoogle ScholarPubMed
Scheewe, T.W., Takken, T., Kahn, R.S., Cahn, W., & Backx, F. (2012). Effects of exercise therapy on cardiorespiratory fitness in patients with schizophrenia. Medicine and Science and Sports and Exercise, 44(10), 18341842.Google ScholarPubMed
Scheewe, T. W., Van Haren, N. E., Sarkisyan, G., Schnack, H. G., Brouwer, R. M., De Glint, M., & Cahn, W. (2013). Exercise therapy, cardiorespiratory fitness and their effect on brain volumes: A randomised controlled trial in patients with schizophrenia and healthy controls. European Neuropsychopharmacology, 23(7), 675685.CrossRefGoogle ScholarPubMed
Sebastião, E., Gobbi, S., Chodzko-Zajko, W., Schwingel, A., Papini, C.B., Nakamura, P.M., & Kokubun, E. (2012). The International Physical Activity Questionnaire-long form overestimates self-reported physical activity of Brazilian adults. Public Health, 126(11), 967975.CrossRefGoogle ScholarPubMed
Snethen, G.A., McCormick, B.P., & Lysaker, P.H. (2014). Physical activity and psychiatric symptoms in adults with schizophrenia spectrum disorders. The Journal of Nervous and Mental Disease, 202(12), 845852.CrossRefGoogle ScholarPubMed
Taylor, C.B., Sallis, J.F., & Needle, R. (1985). The relation of physical activity and exercise to mental health. Public Health Report, 100(2), 195202.Google ScholarPubMed
Taylor, H.L., Buskirk, E., & Henschel, A. (1955). Maximal oxygen intake as an objective measure of cardio-respiratory performance. Journal of Applied Physiology, 8(1), 7380.CrossRefGoogle ScholarPubMed
Van Praag, H. (2008). Neurogenesis and exercise: Past and future directions. Neuromolecular Medicine, 10(2), 128140.CrossRefGoogle ScholarPubMed
Van Praag, H., Christie, B.R., Sejnowski, T.J., & Gage, F.H. (1999). Running enhances neurogenesis, learning, and long-term potentiation in mice. Proceedings of the National Academy of Sciences of the United States of America, 96(23), 1342713431.CrossRefGoogle ScholarPubMed